Do bees know what they don’t know?

When faced with a decision they're likely to get wrong, bees opt out.

Thinking about thinking, or "metacognition," is no easy feat, since it requires self-awareness and reflection. We humans are masters at monitoring our own thoughts, and we can even assess what—and how much—we don't know about something and use this knowledge to inform our decisions. It's called "uncertainty monitoring," and it's a calculation that our brains often do without us even being aware of it.

It's unclear whether other animals also have this ability. Although there is some good evidence demonstratingmetacognition and uncertainty awareness in primates, the extent to which smaller-brained animals can ponder their own cognitive processes is the subject of hot debate in the scientific world.

In this week's issue of PNAS, Clint Perry and Andrew Barron, two Australian researchers, examine uncertainty monitoring in honeybees. Bees are a popular subject for cognitive research, since their brains are relatively simple, and we know quite a bit about how some of their cognitive processes unfold. These reliable little critters are also relatively easy to work with, even outside of the lab.

The researchers created a test chamber with two cylindrical "rooms," each of which held a horizontal reference bar and two targets. Free-flying bees could enter a chamber and drink a solution from one of the two targets inside. However, the location of the targets was a vital signal to the bees; for one group, targets positioned above the reference bar dispensed a sugary solution, and targets below it doled out a bitter quinine solution. For a second group of bees, the targets were reversed. Bees had to choose a target before they were released from the chambers. Not surprisingly, the tiny test subjects quickly learned which targets to avoid and which to drink from.

But the tests got harder when the researchers introduced varying degrees of difficulty. In this phase, some targets were positioned well above or below the reference bar, making the decision obvious. Other targets overlapped the bar but were offset slightly so that the choice was a bit more difficult. Still others were perfectly lined up with the bar so that it was impossible to tell what type of solution would be inside each.

In some trials, bees could simply fly from one chamber into the next without choosing a target, thereby "opting out" of the choice presented to them. In other trials, the exit hole was blocked off, forcing the bees to make a decision about which target to drink from before they were released. If the bees were capable of monitoring their uncertainty, they should opt out more often when the trials were hard, since they lacked enough information to make informed decisions.

And they did: the bees opted out more often when faced with difficult and impossible trials—when the target overlapped the reference bar—than they did on easy trials. The scientists also looked at the differences in performance on forced and unforced trials and found that opting out actually improved the bees' overall performance. The bees were "right" on difficult trials more often when they had the choice of opting out and flying into the other chamber, compared to when they were confined to the choice in the first chamber.

According to Perry and Barron, these results suggest that bees are opting out of trials and cutting their losses when they don't have enough information to make an educated guess. If this is true, it's a pretty significant finding: bees—and potentially other non primates—know when they don't know enough and can react to varying degrees of uncertainty in order to optimize their performance.

But there's another—perhaps simpler—explanation for the bees' behavior. By nature, animals will be wrong more often in difficult trials than they will in easy trials. Since a wrong answer leads to a nasty surprise, the bees may simply be learning to associate harder trials with punishment. In other words, simple associative learning might cause the bees to skip difficult trials in order to avoid the possible penalty.

So which is it? Are bees simply avoiding hard choices because they are more likely to get them wrong, or are they selectively opting out when they don't have enough information?

The answer, as it so often is in science, is that we don't really know yet. The bees did better on unforced than forced trials, suggesting that they were making choices adaptively based on their uncertainty. However, there's still not enough evidence to conclusively say that bees can reflect on, and react to, how much they don't know.

Perry and Barron suggest that a neurobiological model of uncertainty might help clear things up. Once we understand how uncertainty monitoring takes place in the brain, we might be able to develop better ways to rule out associative learning. Additionally, if scientists find that uncertainty awareness isn't very complex biologically, it's less of a stretch to believe that small-brained animals like bees are capable of this strategy.

While it's not hard to understand how and why uncertainty monitoring would be adaptive for honeybees, it isn't necessarily an easy scientific question to answer. In terms of bees' uncertainty, we're still relatively uncertain.

Assume that an individual bee, when faced with the difficult problem, chooses the answer randomly. Allow the same population of bees to repeat such an experiment several times. Some small portion will get the problem right every time and will probably try again when presented with the problem one more time. Some (larger) portion will get the problem wrong often enough to form an association between that problem configuration and "blech". This larger portion will simply associate those particular configurations with punishment, and will therefore behave as they would when subjected to a known noxious stimulus with no proposition of reward.

Repeat the experiment with this population enough times, and eventually you'll converge at some very high portion of the bees (possibly all of them) that are unwilling to try at all.

So the answer here is far less likely that bees are thinking about thinking, or making a calculation of how likely they are to be right (or how difficult the problem is), and far more likely that they are forming several independent associations between different problem configurations and results, and then matching any given newly presented problem to whichever one it looks most like. I doubt that they're even capable of forming a notion of a class of problems that each of these configurations belongs to.

Assume that an individual bee, when faced with the difficult problem, chooses the answer randomly. Allow the same population of bees to repeat such an experiment several times. Some small portion will get the problem right every time and will probably try again when presented with the problem one more time. Some (larger) portion will get the problem wrong often enough to form an association between that problem configuration and "blech". This larger portion will simply associate those particular configurations with punishment, and will therefore behave as they would when subjected to a known noxious stimulus with no proposition of reward.

Repeat the experiment with this population enough times, and eventually you'll converge at some very high portion of the bees (possibly all of them) that are unwilling to try at all.

So the answer here is far less likely that bees are thinking about thinking, or making a calculation of how likely they are to be right (or how difficult the problem is), and far more likely that they are forming several independent associations between different problem configurations and results, and then matching any given newly presented problem to whichever one it looks most like. I doubt that they're even capable of forming a notion of a class of problems that each of these configurations belongs to.

The problem with this idea is that bees have an elaborate method of communication and the clever insects might spoil your test by sharing information.

Funny, when bees opt out of a test, they are considered intelligent. When humans do likewise, they are considered to be feckless losers.

“I divide my officers into four groups. There are clever, diligent, stupid, and lazy officers. Usually two characteristics are combined. Some are clever and diligent -- their place is the General Staff. The next lot are stupid and lazy -- they make up 90 percent of every army and are suited to routine duties. Anyone who is both clever and lazy is qualified for the highest leadership duties, because he possesses the intellectual clarity and the composure necessary for difficult decisions. One must beware of anyone who is stupid and diligent -- he must not be entrusted with any responsibility because he will always cause only mischief.”

Funny, when bees opt out of a test, they are considered intelligent. When humans do likewise, they are considered to be feckless losers.

“I divide my officers into four groups. There are clever, diligent, stupid, and lazy officers. Usually two characteristics are combined. Some are clever and diligent -- their place is the General Staff. The next lot are stupid and lazy -- they make up 90 percent of every army and are suited to routine duties. Anyone who is both clever and lazy is qualified for the highest leadership duties, because he possesses the intellectual clarity and the composure necessary for difficult decisions. One must beware of anyone who is stupid and diligent -- he must not be entrusted with any responsibility because he will always cause only mischief.”

I am not convinced by either the abstract or this summary (and I am too cheap to buy access to the whole paper) that this study can even begin to address the question of whether bees are displaying metacognition.

The evidence presented here seems to be explainable by the visual information being presented failing to elicit any neurological response, with the bees following the rule 'nothing to see here; move along' when they were able to.

The abstract says 'Bees could also transfer the concept of opting out to a novel task.' I wonder how the authors distinguish between 'transfer', and the bees simply defaulting to the same behavior in a different but analogous situation?

If the authors are concerned about a possible explanation based on the bees choosing to avoid the 'punishment' of quinine water, why did they not repeat with plain water? And if finding plain water instead of fake nectar would itself be regarded as 'punishment', then the concept of punishment would seem to have become a redundant tautology - what sort of learning situation would not include it?

By Occam's razor, it seems premature to raise the question of metacognition unless the experiment can throw some light on the question.

I am not convinced by either the abstract or this summary (and I am too cheap to buy access to the whole paper) that this study can even begin to address the question of whether bees are displaying metacognition. ...

I concur.

A paragraph like this: "these results suggest that bees are opting out of trials and cutting their losses when they don't have enough information to make an educated guess" is already anthropomorphising the bees, attributing 'probability/decision weighing' brain circuits.

Couldn't it simply be that below a certainty threshold the bees are simply not induced into drinking behaviour? In nature, a bee often has a huge choice of flowers, and it would be likely that bees evolve what would appear to be a certainty threshold when dealing with flowers: If it smells like a flower that I have good experience with, looks like a flower I have good experience with, and is at the location that was communicated to me, then I'll go ahead and drink. But if it doesn't meet a high enough match of stimuli, the bee's brain simply doesn't respond with a drink behaviour. It has evolved in such a way as to be non-responsive if certainty (smells and vision and location stimuli) doesn't pass a threshold (which is simply how all brain circuits work. If enough neurons fire in a circuit, then the next neurons along that chain get activated and trigger a response in the animal, for example, drink. But if those neurons don't reach the threshold level, it will result in the behaviour not being triggered. But it doesn't mean that the animal has a brain circuit that weighs decisions, simply that the behaviour wasn't induced).

The key with this experiment is that they forced the bees to drink before opening the exit door, and compared that to bees who weren't forced to do something to open the exit. The bee may be learning how to escape, and simply choosing at random, which would result in a lower accuracy for the 'forced to make a decision' bees. I am left concluding that this is not a proof of the bee having metacognition or uncertainty awareness.

That said, I haven't read the paper, so apologies if I'm misunderstanding.

Less well known than the Turing test for artificial intelligence; but I motion that this be referred to as the 'Rumsfeld Test' for metacognition...

" Now what is the message there? The message is that there are no "knowns." There are things we know that we know. There are known unknowns. That is to say there are things that we now know we don't know. But there are also unknown unknowns. There are things we do not know we don't know. So when we do the best we can and we pull all this information together, and we then say well that's basically what we see as the situation, that is really only the known knowns and the known unknowns. And each year, we discover a few more of those unknown unknowns.

It sounds like a riddle. It isn't a riddle. It is a very serious, important matter. "

Just using the term meta-cognition shows the error in their thinking. Cognition, like intelligence, is not a top-down phenomenon. Intelligence is built up, one neuron at a time. Cognition is built up, one neuron at a time. Consciousness is is built up, one neuron at a time. Sentience is built up, one neuron at a time. Everything that we humans can think, has been built up, one neuron at a time.

What is surprising is not that simpler organisms displays some aspects of human thinking, but that scientists seemed surprised when they discover this.

Kate Shaw Yoshida / Kate is a science writer for Ars Technica. She recently earned a dual Ph.D. in Zoology and Ecology, Evolutionary Biology and Behavior from Michigan State University, studying the social behavior of wild spotted hyenas.